RESEARCH ARTICLE Mechanisms Driving Galling Success in a Fragmented Landscape: Synergy of Habitat and Top-Down Factors along Temperate Forest Edges Nina-S. Kelch1, Frederico S. Neves2, G. Wilson Fernandes2,3, Rainer Wirth1* 1 Plant Ecology & Systematics, University of Kaiserslautern, Kaiserslautern, Germany, 2 Departamento de Biologia Geral, Instituto de Ciéncias Biológicas, Universidade Federal de Minas Gerais—UFMG, Belo Horizonte, Minas Gerais, Brazil, 3 Department of Biology, Stanford University, Stanford, California, United States of America * [email protected] a11111 Abstract Edge effects play key roles in the anthropogenic transformation of forested ecosystems and their biota, and are therefore a prime field of contemporary fragmentation research. We present the first empirical study to address edge effects on the population level of a wide- OPEN ACCESS spread galling herbivore in a temperate deciduous forest. By analyzing edge effects on abundance and trophic interactions of beech gall midge (Mikiola fagi Htg.), we found 30% Citation: Kelch N-S, Neves FS, Fernandes GW, Wirth R (2016) Mechanisms Driving Galling Success higher gall abundance in the edge habitat as well as lower mortality rates due to decreased in a Fragmented Landscape: Synergy of Habitat and top-down control, especially by parasitoids. Two GLM models with similar explanatory Top-Down Factors along Temperate Forest Edges. power (58%) identified habitat specific traits (such as canopy closure and altitude) and para- PLoS ONE 11(6): e0157448. doi:10.1371/journal. pone.0157448 sitism as the best predictors of gall abundance. Further analyses revealed a crucial influ- ence of light exposure (46%) on top-down control by the parasitoid complex. Guided by a Editor: Louis-Felix Bersier, University of Fribourg, SWITZERLAND conceptual framework synthesizing the key factors driving gall density, we conclude that forest edge proliferation of M. fagi is due to a complex interplay of abiotic changes and tro- Received: February 12, 2016 phic control mechanisms. Most prominently, it is caused by the microclimatic regime in for- Accepted: May 31, 2016 est edges, acting alone or in synergistic concert with top-down pressure by parasitoids. Published: June 16, 2016 Contrary to the prevailing notion that specialists are edge-sensitive, this turns M. fagi into a Copyright: © 2016 Kelch et al. This is an open winner species in fragmented temperate beech forests. In view of the increasing proportion access article distributed under the terms of the of edge habitats and the documented benefits from edge microclimate, we call for investiga- Creative Commons Attribution License, which permits tions exploring the pest status of this galling insect and the modulators of its biological unrestricted use, distribution, and reproduction in any medium, provided the original author and source are control. credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information file. Funding: The authors received no specific funding for this work. Introduction Competing Interests: The authors have declared Forest fragmentation is ranked amongst the leading mechanism behind the current global bio- that no competing interests exist. diversity crisis and belongs to the most pervasive impacts of human land use [1,2]. As a PLOS ONE | DOI:10.1371/journal.pone.0157448 June 16, 2016 1/17 Forest Edge Effects on Galling Insects consequence of ongoing fragmentation, human-modified landscapes are now faced with an escalating proportion of edge habitats at the expense of continuous forest interior [3,4]. The resulting edge effects play key roles in the anthropogenic transformation of forested ecosystems and their biota, and are therefore a prime field of contemporary fragmentation research [5–8]. Currently, edge-induced alterations of species interactions receive particular close attention and there is considerable research effort underway to evaluate both the nature and intensity of these changes as well as cascading ecological consequences throughout a web of relationships. In fact, the disruption of trophic interactions has been repeatedly identified as a key mecha- nism involved in edge-mediated loss of ecosystem function or biodiversity [9–11] yet the understanding of the underlying causal processes is often sketchy. Among all trophic relation- ships, insect herbivory is widely recognized as one of the key processes shaping plant commu- nities and influencing ecosystem function [12,13]. A general trend observed within the edge literature is a positive response of herbivores to forest edges. Especially generalist herbivores benefit from favorable micro-environmental conditions, increased food quantity and quality, including higher nutrition content and less defense capacity of plant tissue [8]. They may also profit from a disrupted top-down regulation, yet this is less well documented [11]. However, while several studies showed a clear profit of generalist herbivores to edge-driven changes, empirical evidence on specialized herbivores is less clear [8]. Due to their sessile life style and their high degree of host-specificity, gallers are regarded as particularly promising target taxa to compare the influence of different factors in a spatial con- text, and link cause to effect [14]. Limited research exists, however, investigating edge effects on gallers, most of it concentrating on gall diversity rather than species specific responses [15– 18]. In fact, to our knowledge there is no study available addressing anthropogenic edge effect on gall species at the population level (see [16] for a study across a natural ecotone). Here we used the galling insect–host plant system Fagus sylvatica L. (European beech) and Mikiola fagi Htg. (beech gall midge; Diptera: Cecidomyiidae). This species pair provides an excel- lent model system for our work for the following reasons. The beech gall midge induces egg- shaped, unilarval galls [19], which are shed (before leaf fall) for overwintering in the leaf litter. It is the most common and important herbivore species associated with beech [20,21] and there is considerable knowledge available about factors regulating its population density, ranging from (i) top-down control through a parasitoid complex [20, 22], and gall predation (e.g., by birds [23]), to (ii) bottom-up induced plant defense, called hypersensitivity reaction (HR) by the host tree F. sylvatica [24], and (iii) environmental conditions, such as increased gall infestation rates follow- ing high light exposure [25]. On the other hand, F. sylvatica is among the most abundant and economically important broad-leaved trees in the northern hemisphere and a key element of the European beech forest [26]—a unique European ecosystem with global conservation value as reflected by its UNESCO world natural heritage status [27]. The relevance of fragmentation- related studies on these forests is emphasized by the remarkable dominance and shade casting ability of beech [28]. As a result, the contrast between beech forest interior and edge is expected to be more abrupt compared to structurally more heterogeneous forest types. In this paper we aimed at a detailed assessment of edge impacts and underlying mechanisms on the beech–gall midge system by collecting habitat-, resource-, and top-down-related data from the individual tree to the stand level and sampling over 10.000 galls on more than 300 individual beech trees across a fragmented beech forest landscape. We hypothesized that at the forest edge M. fagi galls (1) are more abundant because of their documented preference for light-exposed sites and (2) benefit from disrupted top-down control exerted by parasitoids, as implied by the trophic-level hypothesis of island biogeography (i.e. populations of higher tro- phic levels are more likely to become extinct under fragmentation conditions [29]) and empiri- cal evidence for edge sensitivity of parasitoids [8]. To identify possible links and interactions PLOS ONE | DOI:10.1371/journal.pone.0157448 June 16, 2016 2/17 Forest Edge Effects on Galling Insects between gall density, characteristic habitat traits, and biotic factors, we adopted several statisti- cal models and, finally, generated a conceptual model that synthesizes key factors driving gall density across fragmented beech forest landscapes. Materials and Methods Study region and target species The study was conducted in the Northern Palatinate Highlands (Fig 1, a low mountain range (250–687 m ASL) in SW Germany (federal state of Rhineland-Palatinate). No endangered or protected species were involved. Permission to conduct the study in the respective forest areas was given by the Rhineland-Palatinate Ministry for Environment, Agriculture, Nutrition, Viti- culture and Forestry. Carboniferous and Permian bedrock and sediments as well as Rotliegend volcanic rocks give distinction to the undulating landscape [30]. The climate is temperate and under oceanic influence with average temperatures ranging from of 8–9°C and mean annual precipitation from 550–800 mm [31]. The region is a human-modified landscape consisting of a mosaic of land uses and covers. Forests are deciduous, broad-leaved woodlands (Carpino-Fagetalia mixed forests) and have been subjected to extensive deforestation dating back to the Middle Ages. Land use is concen- trated in sand and siltstone-dominated valleys, while the agriculturally less valuable igneous hilltops remain mostly forested. This fragmentation history has resulted in a landscape of hyper-fragmented